Journal of Chemical Ecology

, Volume 37, Issue 7, pp 741–750

Identification of Semiochemicals Released by Cotton, Gossypium hirsutum, Upon Infestation by the Cotton Aphid, Aphis gossypii

  • Mahabaleshwar Hegde
  • Janser N. Oliveira
  • Joao G. da Costa
  • Ervino Bleicher
  • Antonio E. G. Santana
  • Toby J. A. Bruce
  • John Caulfield
  • Sarah Y. Dewhirst
  • Christine M. Woodcock
  • John A. Pickett
  • Michael A. Birkett


The cotton aphid, Aphis gossypii (Homoptera: Aphididae), is increasing in importance as a pest worldwide since the introduction of Bt-cotton, which controls lepidopteran but not homopteran pests. The chemical ecology of interactions between cotton, Gossypium hirsutum (Malvaceae), A. gossypii, and the predatory lacewing Chrysoperla lucasina (Neuroptera: Chrysopidae), was investigated with a view to providing new pest management strategies. Behavioral tests using a four-arm (Pettersson) olfactometer showed that alate A. gossypii spent significantly more time in the presence of odor from uninfested cotton seedlings compared to clean air, but significantly less time in the presence of odor from A. gossypii infested plants. A. gossypii also spent significantly more time in the presence of headspace samples of volatile organic compounds (VOCs) obtained from uninfested cotton seedlings, but significantly less time with those from A. gossypii infested plants. VOCs from uninfested and A. gossypii infested cotton seedlings were analyzed by gas chromatography (GC) and coupled GC-mass spectrometry (GC-MS), leading to the identification of (Z)-3-hexenyl acetate, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), methyl salicylate, and (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), which were produced in larger amounts from A. gossypii infested plants compared to uninfested plants. In behavioral tests, A. gossypii spent significantly more time in the control (solvent) arms when presented with a synthetic blend of these four compounds, with and without the presence of VOCs from uninfested cotton. Coupled GC-electroantennogram (EAG) recordings with the lacewing C. lucasina showed significant antennal responses to VOCs from A. gossypii infested cotton, suggesting they have a role in indirect defense and indicating a likely behavioral role for these compounds for the predator as well as the aphid.

Key Words

Gossypium hirsutum Aphis gossypii Chrysoperla lucasina Cotton Induced defense Olfactometer EAG Repellency (Z)-3-Hexenyl acetate (E)-4,8-Dimethyl-1,3,7-nonatriene Methyl salicylate (E,E)-4,8,12-Trimethyl-1,3,7,11-tridecatetraene 


  1. Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949.CrossRefGoogle Scholar
  2. Anonymous, 2010. Bt cotton boosting pesticide use, G.M. News Genetic Engineering, GM Food and GM Crops News. Tuesday, 16 February 2010.Google Scholar
  3. Birkett, M. A., Campbell C. A. M., Chamberlain, K., Guerrieri, E., Hick, A. J., Martin, J. L., Matthes, M., Napier, J. A., Pettersson, J., Pickett, J. A., Poppy, G. M., Pow, E. M., Pye, B. J., Smart, L. E., Wadhams, G. H., Wadhams, L. J., and Woodcock, C. M. 2000. New roles for cis-jasmone as an insect semiochemical and in plant defense. Proc. Natl. Acad. Sci. USA 97:9329–9334.CrossRefPubMedGoogle Scholar
  4. Biswas, S., and Singh, R. 1998. Interaction between host plant resistance and the biocontrol of a cereal aphid. Biol. Agric. Hortic. 16:25–36.Google Scholar
  5. Blua, M. J., and Perring, T. M. 1992. Effects of Zucchini Yellow Mosaic Virus on colonization and feeding behavior of Aphis gossypii (Homoptera: Aphididae) Alatae. Environ. Entomol. 21:578–585.Google Scholar
  6. Bruce, T. J. A., and Pickett, J. A. 2007. Plant defence signalling induced by biotic attacks. Curr. Opin. Plant Biol. 10:387–392.CrossRefPubMedGoogle Scholar
  7. Bruce, T. J. A., Martin, J. L., Pickett, J. A., Pye, B. J., Smart, L. E., and Wadhams, L. J. 2003. cis-Jasmone treatment induces resistance in wheat plants against the grain aphid, Sitobion avenae (Fabricius) (Homoptera: Aphididae). Pest Man. Sci. 59:1031–1036.CrossRefGoogle Scholar
  8. Bruce, T. J. A., Wadhams, L. J., and Woodcock, C. M. 2005. Insect host location: a volatile situation. Trends Plant Sci. 10:269–274.CrossRefPubMedGoogle Scholar
  9. Bruce, T. J. A., Matthes, M., Chamberlain, K., Woodcock, C. M., Mohib, A., Webster, B., Smart, L. E., Birkett, M. A., Pickett, J. A., and Napier, J. A. 2008. Multitropic interactions involving Arabadopsis thaliana investigated by means of cis-jasmone defence activation. Proc. Natl. Acad. Sci. USA 105:4553–4558.CrossRefPubMedGoogle Scholar
  10. Canard, M. 2001. Natural food and feeding habits of lacewings, pp. 116–128, in P. K. McEwen, T. R. New and A. Whittington (eds.). Lacewings in the Crop Environment. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  11. Da Costa, J. G., Pires, E. V., Riffel, A., Birkett, M. A., Bleicher, E., and Goulart Sant’Ana, A. E. (2011). Differential preference of Capsicum spp. cultivars by Aphis gossypii is conferred by variation in volatile semiochemistry. Euphytica 177:299–307.CrossRefGoogle Scholar
  12. Degenhardt, J., Kollner, T. G., and Gershenzon, J. 2009. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70:1621–1637.CrossRefPubMedGoogle Scholar
  13. Du, Y., Poppy, G. M., Powell, W. Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1998. Identification of semiochemicals released during aphid feeding that attract the parasitoid Aphidius ervi. J. Chem. Ecol. 24:1355–1368.CrossRefGoogle Scholar
  14. Elmer, H. S., and Brawner, O. L. 1975. Control of brown soft scale in Central Valley. Citrograph 60:402–403.Google Scholar
  15. Francki, R. I. B., Mossop, D. W., and Hatta. T. 1979. Cucumber mosaic virus. CMI/AAB Descriptions of Plant Viruses. No. 213.Google Scholar
  16. Frey, M., Stettner, C., Pare, P. W., Schmelz, E. A., Tumlinson, J. H., and Gierl, A. 2000. An herbivore elicitor activates the gene for indole emission in maize. Proc. Natl. Acad. Sci. USA 97:14801–1806.CrossRefPubMedGoogle Scholar
  17. Frost, C. J., Mescher, M. C., Dervinis, C., Davis, J. M., Carlson, J. E., and De Moraes, C. M. 2008. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol. 180:722–734.CrossRefPubMedGoogle Scholar
  18. Hardie, J., Isaacs, R., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M. 1994. Methyl salicylate and (−)-(1R,5S)-myrtenal are plant-derived repellents for black bean aphid, Aphis fabae (Homoptera: Aphididae). J. Chem. Ecol. 20:2847–2855.CrossRefGoogle Scholar
  19. Herde, M., Gartner, K., Kollner, T. G., Fode, B., Boland, W., Gershenzon, J., Gatz, C., and Tholl, D. 2008. Identification and regulation of TPS04/GES, an Arabidopsis geranyllinalool synthase catalysing the first step in the formation of the insect-induced volatile C16-homoterpene TMTT. Plant Cell 20:1152–1168.CrossRefPubMedGoogle Scholar
  20. Herron, G. A., and Wilson, L. J. 2010. Neonicotinoid resistance in Aphis gossypii Glover (Aphididae: Hemiptera) from Australian cotton. Aust. J. Entomol. 50:93–98.CrossRefGoogle Scholar
  21. Herron, G. A., Powis, K., and Rophail, J. 2001. Insecticide resistance in Aphis gossypii Glover (Hemiptera: Aphididae), a serious threat to Australian cotton. Aust. J. Entomol. 40:85–91.CrossRefGoogle Scholar
  22. James, D. G., Castle, S. C., Grasswitz, T., and Reyna, V. 2005. Using synthetic herbivore-induced plant volatile to enhance conservation biological control: field experiments in hops and grapes. Proc.2nd Int. Symp. Biol. Cont. Arthr. I:192–205.Google Scholar
  23. Kerns, D. L., and Gaylor, M. J. 1992. Insecticide resistance in field populations of the cotton aphid (Homoptera: Aphididae). J. Econ. Entomol. 85:1–8.Google Scholar
  24. Kharbouti, M. S., and Allen, C. T. 2000. Comparison of insecticides for cotton aphid control, pp. 129–131, in Proceedings of the Cotton Research Meeting Arkansas Agricultural Experiment Station, Fayetteville, Arkansas 72701.Google Scholar
  25. Klingler, J., Kovalski, I., Silberstein, L., Thompson, G. A., and Rafael, P. T. 2001. Mapping of cotton-melon aphid resistance in melon. J. Amer. Soc. Hort. Sci. 126:56–63.Google Scholar
  26. Koczor, S., Szentkiralyi, F., Birkett, M. A., Pickett, J. A., Voigt, E., and Toth, M. 2010. Attraction of Chrysoperla carnea complex and Chrysopa spp. lacewings (Neuroptera: Chrysopidae) to aphid sex pheromone components and a synthetic blend of floral compounds in Hungary, Pest Man. Sci. 66:1374–1379.CrossRefGoogle Scholar
  27. Landis, D. A., Wratten, S. D., and Geoff, M. G. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 45:175–201.CrossRefPubMedGoogle Scholar
  28. Lee, S., Badieyan, S., Bevan, D. R., Herde, M., Gatz, C., and Tholl, D. 2010. Herbivore-induced and floral homoterpene volatiles are biosynthesized by a single P450 enzyme (CYP82G1) in Arabidopsis. Proc. Natl. Acad. Sci. USA 107:21205–21210.CrossRefPubMedGoogle Scholar
  29. Leopold, E. J. 1990. Selective hydroboration of a 1,3,7-triene: homogeraniol. Org Synth. 64:164–171.Google Scholar
  30. Loughrin, J. H., Manukian, A., Heath, R. R., Turlings, T. C. J., and Tumlinson, J. H. 1994. Diurna1 cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc. Natl. Acad. Sci. USA 91:11836–11840.CrossRefPubMedGoogle Scholar
  31. Lu, Y., Wu, K., Jiang, Y., Xia, B., Li, P., Feng, H., Wyckhuys, K. G., and Guo, Y. 2010. Mirid bug outbreaks in multiple crops correlated with wide-scale adoption of Bt cotton in China in long-term ecological effects of transgenic Bacillus thuringiensis (Bt) crops on nontarget. Science 328:1151–1154.CrossRefPubMedGoogle Scholar
  32. Maddrell, S. H. P. 1969. Secretion by the Malphigian tubules of Rhodnius. The movement of ions and water. J. Exp. Biol. 51:71–97.Google Scholar
  33. Matthes, M., Bruce, T., Ton, J., Verrier, P. J., Pickett, J. A., and Napier, J. A. 2010. The transcriptome of cis-jasmone-induced resistance in Arabidopsis thaliana and its role in indirect defence. Planta 232:1163–1180.CrossRefPubMedGoogle Scholar
  34. Matthes, M., Bruce, T., Chamberlain, K., Pickett, J., and Napier, J. 2011. Emerging roles in plant defense for cis-jasmone-induced cytochrome P450 CYP81D11. Plant Signal. Behav. 6:1–3.CrossRefGoogle Scholar
  35. Mccall, P. J., Turlings, T. C. J., Loughrin, J., Proveaux, A. T., and Tumlinson, J. H. 1994. Herbivore-induced volatile emissions from cotton (Gossypium hirsutum L.) seedlings. J. Chem. Ecol. 20:3039–3050.CrossRefGoogle Scholar
  36. Moraes, M. C. B., Sereno, F. T. P. S., Michereff, M. F. F., Pareja, M., Laumann, R. A., Birkett, M. A., Pickett, J. A., and Borges, M. 2009. Attraction of the stink bug egg parasitoid Telenomus podisi (Hymenoptera Scelionidae) to defence signals from soybean, Glycine max (Fabaceae), activated by treatment with cis-jasmone. Entomol. Exp. Appl. 131:178–188.CrossRefGoogle Scholar
  37. NIST 2005. NIST mass spectral search for the NIST/EPA/NIH mass spectral library version 2.0. Office of the Standard Reference Data Base, National Institute of Standards and Technology, Gaithersburg, Maryland.Google Scholar
  38. Pettersson, J., Pickett, J. A., Pye, B. J., Quiroz, A., Smart, L. E., Wadhams, L. J., and Woodcock, C. M. 1994. Winter host component reduces colonisation by bird cherry–oat aphid, Rhopalosiphum padi (L.) (Homoptera, Aphididae), and other aphids in cereal fields. J. Chem. Ecol. 20:2565–2574.CrossRefGoogle Scholar
  39. Pickett, J. A. 1990. Gas chromatography–mass spectrometry in insect pheromone identification: three extreme cases, pp. 209–309, in A. R. McCaffery and I. D. Wilson (eds.). Chromatography and Isolation of Insect Pheromones and Hormones. Plenum, New York.Google Scholar
  40. Pickett, J. A., and Poppy, G. M. 2001. Switching on plant genes by external chemical signals. Trends Plant Sci. 6:137–139.CrossRefPubMedGoogle Scholar
  41. Qaim, M., and De Janvry, A. 2005. Bt cotton and pesticide use in Argentina: economic and environmental effects. Environ. Dev. Econ. 10:179–200.CrossRefGoogle Scholar
  42. Reay-Jones, F. P. F., Toews, M. D., Greene, J. K., and Reeves, R. B. 2010. Development of sampling plans for cotton bolls injured by stink bugs (Hemiptera: Pentatomidae). J. Econ. Entomol. 103:525–532.CrossRefPubMedGoogle Scholar
  43. Rodriguez-Saona, C., Crafts-Brandner, S. J., and Canas, L. A. 2003. Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J. Chem. Ecol. 29:2539–2550.CrossRefPubMedGoogle Scholar
  44. Rose, U. S., and Tumlinson, J. H. 2005. Systemic induction of volatile release in cotton: How specific is the signal to herbivory. Planta 222:327–335.CrossRefPubMedGoogle Scholar
  45. Rose, U. S., Manukian, A., Heath, R. R., and Tumlinson, J. H. 1996. Volatile semiochemicals released from undamaged cotton leaves: a systemic response of living plants to caterpillar damage. Plant. Physiol. 111:487–495.PubMedGoogle Scholar
  46. Rosenheim, J. A., and Wilhoit, L. R. 1993. Why lacewings may fail to suppress aphids predators that eat other predators disrupt cotton aphid control. Calif. Agr. 47:7–9.Google Scholar
  47. Ross, J. R., Nam, K. H., Dauria, J. C., and Pichersky, E. 1999. S-adenosyl—methionine : salicylic acid carboxyl methyltransferase an enzyme involved in floral scent production and plant defence, represents a new class of plant methyltransferases. Arch. Biochem. Biophys. 367:9.CrossRefPubMedGoogle Scholar
  48. Seelan, T., Schnabal, A., and Wendel, J. F. 1997. Congruence and consensus in the cotton tribe (Malvaceae). Syst. Bot. 22:259–290.CrossRefGoogle Scholar
  49. Siebert, M. W., Leonard, B. R., Gable, R. H., and Lamotte, L. R. 2005. Cotton boll age influences feeding preference by brown stink bug (Heteroptera: Pentatomidae). J. Econ. Entomol. 98:82–87.CrossRefPubMedGoogle Scholar
  50. Skelton, A. C., Cameron, M. M., Pickett, J. A., and Birkett, M. A. 2010. Identification of neryl formate as an airborne aggregation pheromone for the American house dust mite, Dermatophagoides farinae, and the European house dust mite, Dermatophagoides pteronyssinus (Acari: Epidermoptidae). J. Med. Entomol. 47:798–804.CrossRefPubMedGoogle Scholar
  51. Snoeren, T. A. L., Kappers, I. F., Broekgaarden, C., Mumm, R., Dicke, M., and Bouwmeester, H. J. 2010. Natural variation in herbivore-induced volatiles in Arabidopsis thaliana. J. Exp. Bot. 61:3041–3056.CrossRefPubMedGoogle Scholar
  52. Stein, A. 2001. Survey of Ghaggar- Hakra River, 1940–42, pp. 277–280, in C. Jarrige and V. Lefevre (eds.). South Asian ArchaeologyGoogle Scholar
  53. Wadhams, L. J. 1990. The use of coupled gas chromatography: electrophysiological techniques in the identification of insect pheromones, pp. 289–298, in A. R. McCaffery and I. D. Wilson (eds.). Chromatography and Isolation of Insect Hormones and Pheromones. Plenum, New York.Google Scholar
  54. Webster, B., Bruce, T., Dufour, S., Birkemeyer, C., Birkett, M., Hardie, J., and Pickett, J. 2008. Identification of volatile compounds used in host location by the black bean aphid, Aphis fabae. J. Chem. Ecol. 34:1153–1161.CrossRefPubMedGoogle Scholar
  55. Webster, B., Bruce, T., Pickett, J., and Hardie, J. 2010. Volatiles functioning as host cues in a blend become non-host cues when presented alone to the black bean aphid. Anim. Behav. 79:451–457.CrossRefGoogle Scholar
  56. Wendel, J. F., and Albert, V. A. 1992. Phylogenetics of the cotton genus (Gossypium) character-state weighted parasimony analysis of chloroplast DNA restriction site data its systematic and biogeographic implications. Syst. Bot. 17:115–143.CrossRefGoogle Scholar
  57. Willrich, M. M., Leonard, B. R., and Padgett, G. B. 2004a. Influence of southern green stink bug, Nezara viridula L., on late-season yield losses in cotton, Gossypium hirsutum L. Environ. Entomol. 33:1095–1101.CrossRefGoogle Scholar
  58. Willrich, M. M., Leonard, B. R., Gable, R. H., and Lamotte, L. R. 2004b. Boll injury and yield losses in cotton associated with brown stink bug (Heteroptera: Pentatomidae) during flowering. J. Econ. Entomol. 97:1928–1934.CrossRefPubMedGoogle Scholar
  59. Willrich, M. M., Leonard, B. R., and Temple, J. 2004c. Injury to preflowering and flowering cotton by brown stink bug and southern green stink bug. J. Econ. Entomol. 97:924–933.CrossRefPubMedGoogle Scholar
  60. Wu, K. M., Lu, Y. H., Feng, H. Q., Jiang, Y. Y., and Zhao, J. Z. 2008. Suppression of cotton bollworm in multiple crops in China in areas with Bt toxin–containing cotton. Science 321:1676–1678.CrossRefPubMedGoogle Scholar
  61. Xia, J. 1997. Biological control of cotton aphid (Aphis gossypii Glover) in cotton (inter)cropping systems in China: a simulation study. PhD Thesis. Wageningen University. Netherland 173p.Google Scholar
  62. Zhu, J., and Park, K. C. 2005. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J. Econ. Entomol. 31:1733–1746.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Mahabaleshwar Hegde
    • 1
  • Janser N. Oliveira
    • 3
  • Joao G. da Costa
    • 4
  • Ervino Bleicher
    • 3
  • Antonio E. G. Santana
    • 5
  • Toby J. A. Bruce
    • 2
  • John Caulfield
    • 2
  • Sarah Y. Dewhirst
    • 2
  • Christine M. Woodcock
    • 2
  • John A. Pickett
    • 2
  • Michael A. Birkett
    • 2
  1. 1.Department of Agricultural EntomologyUniversity of Agricultural SciencesDharwadIndia
  2. 2.Biological Chemistry DepartmentRothamsted ResearchHarpendenUK
  3. 3.Departamento de FitotecniaUniversidade Federal do Ceará (UFC)FortalezaBrazil
  4. 4.Embrapa Tabuleiros Costeiros, Tabuleiro do MartinsMaceióBrazil
  5. 5.Instituto de Química e BiotecnologiaUniversidade Federal de AlagoasMaceióBrazil

Personalised recommendations